Role for estradiol in female-typical brain and behavioral sexual differentiation

Frontiers in Neuroendocrinology

Volumn 29, Issue 1, 2008, Pages 1-16

  Bakker, Julie ^a   Baum, Michael J ^b  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b Boston University   (United States)

Author keywords

Fetoprotein; Aromatase; Brain; Estrogens; Sexual behavior; Sexual differentiation

Indexed keywords

ALPHA FETOPROTEIN; AROMATASE; ESTRADIOL;

BRAIN DEVELOPMENT; ESTROGEN ACTIVITY; FEMINIZATION; KNOCKOUT MOUSE; NEUROENDOCRINOLOGY; NEUROPROTECTION; NONHUMAN; PRENATAL PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REVIEW; SEX DIFFERENTIATION; SEXUAL BEHAVIOR;

ALPHA-FETOPROTEINS; ANIMALS; AROMATASE; BRAIN; ESTRADIOL; FEMALE; HUMANS; INFERTILITY, FEMALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; SEX DIFFERENTIATION; SEXUAL BEHAVIOR;

EID: 37549055112     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2007.06.001     Document Type: Review

References (116)

1. Abelev G.I., Perova S.D., Khramkova N.I., Postnikova Z.A., and Irlin I.S. Production of embryonal alpha-globulin by transplantable mouse hepatomas. Transplantation 1 (1963) 174-180
2. Ali M., Mujoo K., and Sahib M.K. Synthesis and secretion of alpha-fetoprotein and albumin by newborn rat brain cells in culture. Brain Res. 282 (1982) 47-55
3. Andrews G.K., Dziadek M., and Tamaoki T. Expression and methylation of the mouse alpha-fetoprotein gene in embryonic, adult, and neoplastic tissues. J. Biol. Chem. 257 (1982) 5148-5153
4. Arnon R., Teicher E., Bustin M., and Sela M. Preparation of antisera to alpha-fetoprotein making use of estradiol affinity column. FEBS Lett. 32 (1973) 335-338
5. Aussel C., and Masseyeff R. Rat alpha-fetoprotein-estrogen interaction. J. Steroid Biochem. 9 (1978) 547-551
6. Bakker J., De Mees C., Douhard Q., Balthazart J., Gabant P., Szpirer J., and Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat. Neurosci. 9 (2006) 220-226
7. Bakker J., De Mees C., Szpirer J., Szpirer C., and Balthazart J. Exposure to oestrogen prenatally does not interfere with the normal female-typical development of odour preferences. J. Neuroendocrinol. 19 (2007) 329-334
8. Bakker J., Honda S., Harada N., and Balthazart J. The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J. Neurosci. 22 (2002) 9104-9112
9. Bakker J., Honda S., Harada N., and Balthazart J. Restoration of male sexual behavior by adult exogenous estrogens in male aromatase knockout mice. Horm. Behav. 46 (2004) 1-10
10. Baum M.J. Differentiation of coital behavior in mammals: a comparative analysis. Neurosci. Biobehav. Rev. 3 (1979) 265-284
11. Baum M.J., and Keverne E.B. Sex difference in attraction thresholds for volatile odors from male and estrous female mouse urine. Horm. Behav. 41 (2002) 213-219
12. Baum M.J., and Tobet S.A. Effect of prenatal exposure to aromatase inhibitor, testosterone, or antiandrogen on the development of feminine sexual behavior in ferrets of both sexes. Physiol. Behav. 37 (1986) 111-118
13. Bennett J.A., DeFreest L., Anaka I., Saadati H., Balulad S., Jacobson H.I., and Andersen T.T. AFPep: an anti-breast cancer peptide that is orally active. Breast Cancer Res. Treat. 98 (2006) 133-141
14. Bennett J.A., Mesfin F.B., Andersen T.T., Gierthy J.F., and Jacobson H.I. A peptide derived from alpha-fetoprotein prevents the growth of estrogen-dependent human breast cancers sensitive and resistant to tamoxifen. Proc. Natl. Acad. Sci. USA 99 (2002) 2211-2215
15. Bergstrand C.G., and Czar B. Demonstration of a new protein fraction in serum from the human fetus. Scand. J. Clin. Lab. Invest. 8 (1956) 174
16. Blizard D., and Denef C. Neonatal androgen effects on open-field activity and sexual behavior in the female rat: the modifying influence of ovarian secretions during development. Physiol. Behav. 11 (1973) 65-69
17. Bodo C., and Rissman E.F. Androgen receptor is essential for sexual differentiation of responses to olfactory cues in mice. Eur. J. Neurosci. 25 (2007) 2182-2190
18. Booth J.E. Sexual differentiation of the brain. In: Finn C.A. (Ed). Oxford Reviews of Reproductive vol. I (1979), Clarendon Press, Oxford 58-158 Ref Type: Serial (Book,Monograph)
19. Brownbill P., Edwards D., Jones C., Mahendran D., Owen D., Sibley C., Johnson R., Swanson P., and Nelson D.M. Mechanisms of alphafetoprotein transfer in the perfused human placental cotyledon from uncomplicated pregnancy. J. Clin. Invest. 96 (1995) 2220-2226
20. Clark A.S., Pfeifle J.K., and Edwards D.A. Ventromedial hypothalamic damage and sexual proceptivity in female rats. Physiol. Behav. 27 (1981) 597-602
21. M.A. Crawford, A.J. Sinclair, Nutritional influences in the evolution of the mammalian brain, in: CIBA Foundation Symposium, Churchill London, Malnutrition and the Developing Brain, 1972, pp. 267-287.
22. Cuckle H.S., Wald N.J., and Lindenbaum R.H. Maternal serum alpha-fetoprotein measurement: a screening test for Down syndrome. Lancet 1 (1984) 926-929
23. Daniels D., Miselis R.R., and Flanagan-Cato L.M. Central neuronal circuit innervating the lordosis-producing muscles defined by transneuronal transport of pseudorabies virus. J. Neurosci. 19 (1999) 2823-2833
24. De Mees C., Laes J.F., Bakker J., Smitz J., Hennuy B., Van Vooren P., Gabant P., Szpirer J., and Szpirer C. Alpha-fetoprotein controls female fertility and prenatal development of the gonadotropin-releasing hormone pathway through an antiestrogenic action. Mol. Cell. Biol. 26 (2006) 2012-2018
25. De Vries G.J., Rissman E.F., Simerly R.B., Yang L.Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., and Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J. Neurosci. 22 (2002) 9005-9014
26. Dohler K.D., Hancke J.L., Srivastava S.S., Hofmann C., Shryne J.E., and Gorski R.A. Participation of estrogens in female sexual differentiation of the brain; neuroanatomical, neuroendocrine and behavioral evidence. In: De Vries G.J., De Bruin J.P.C., Uylings H.B.M., and Corner M.A. (Eds). Progress in Brain Research. Sex differences in the brain, the relation between structure and function 61 (1984), Elsevier, Amsterdam 99-117 Ref Type: Serial (Book,Monograph)
27. Dorner G. Sexual differentiation of the brain. Vitam. Horm. 38 (1981) 325-381 Ref Type: Serial (Book,Monograph)
28. Dorries K.M., Adkins-Regan E., and Halpern B.P. Olfactory sensitivity to the pheromone, androstenone, is sexually dimorphic in the pig. Physiol. Behav. 57 (1995) 255-259
29. Dunlap J.L., Gerall A.A., and McLean L.D. Enhancement of female receptivity in neonatally castrated males by prepuberal ovarian transplants. Physiol. Behav. 10 (1973) 701-705
30. Edwards D.A., and Burge K.G. Olfactory control of the sexual behavior of male and female mice. Physiol. Behav. 11 (1973) 867-872
31. Feder H.H., and Whalen R.E. Feminine behavior in neonatally castrated and estrogen-treated male rats. Science 147 (1965) 306-307
32. Firestein S. How the olfactory system makes sense of scents. Nature 413 (2001) 211-218
33. Fisher C.R., Graves K.H., Parlow A.F., and Simpson E.R. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc. Natl. Acad. Sci. USA 95 (1998) 6965-6970
34. Gabant P., Forrester L., Nichols J., Van Reeth T., De Mees C., Pajack B., Watt A., Smitz J., Alexandre H., Szpirer C., and Szpirer J. Alpha-fetoprotein, the major fetal serum protein, is not essential for embryonic development but is required for female fertility. Proc. Natl. Acad. Sci. USA 99 (2002) 12865-12870
35. Gerall A.A., Dunlap J.L., and Hendricks S.E. Effect of ovarian secretions on female behavioral potentiality in the rat. J. Comp. Physiol. Psychol. 82 (1973) 449-465
36. Gibori G., and Sridaran R. Sites of androgen and estradiol production in the second half of pregnancy in the rat. Biol. Reprod. 24 (1981) 249-256
37. Gillespie J.R., and Uversky V.N. Structure and function of alpha-fetoprotein: a biophysical overview. Biochim. Biophys. Acta 1480 (2000) 41-56
38. Gorski R.A., and Jacobson C.D. Sexual differentiation of the brain. In: Kogan S.E., and Hafez E.S.E. (Eds). Pediatric Andrology (1981), Martinus Nijfhoff, The Hague, The Netherlands 109-134 Ref Type: Serial (Book,Monograph)
39. Goy R.W., and McEwen B.S. Sexual Differentiation of the Brain (1980), Masachusettes Institute of Technology Press, Cambridge MA, USA Ref Type: Serial (Book,Monograph)
40. Grady K.L., Phoenix C.H., and Young W.C. Role of the developing rat testis in differentiation of the neural tissues mediating mating behavior. J. Comp. Physiol. Psychol. 59 (1965) 176-182
41. Greco T.L., and Payne A.H. Ontogeny of expression of the genes for steroidogenic enzymes P450 side-chain cleavage, 3 beta-hydroxysteroid dehydrogenase, P450 17 alpha-hydroxylase/C17-20 lyase, and P450 aromatase in fetal mouse gonads. Endocrinology 135 (1994) 262-268
42. Haddow J.E., Macri J.N., and Munson M. The amnion regulates movement of fetally derived alpha-fetoprotein into maternal blood. J. Lab. Clin. Med. 94 (1979) 344-347
43. Han T.M., and De Vries G.J. Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J. Neurobiol. 54 (2003) 502-510
44. Honda S., Harada N., Ito S., Takagi Y., and Maeda S. Disruption of sexual behavior in male aromatase-deficient mice lacking exons 1 and 2 of the cyp19 gene. Biochem. Biophys. Res. Commun. 252 (1998) 445-449
45. Jost A. Sur le contrôle hormonal de différenciation sexuelle du lapin. Arch. Anat. Microscop. Morphol. Exp. 39 (1950) 577-598
46. Keller M., Douhard Q., Baum M.J., and Bakker J. Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chem. Senses 31 (2006) 315-323
47. Keller M., Pierman S., Douhard Q., Baum M.J., and Bakker J. The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. Eur. J. Neurosci. 23 (2006) 521-530
48. Keverne E.B. The vomeronasal organ. Science 286 (1999) 716-720
49. Kimoto H., Haga S., Sato K., and Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437 (2005) 898-901
50. Koopman P., Munsterberg A., Capel B., Vivian N., and Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testis differentiation. Nature 348 (1990) 450-452
51. Kudwa A.E., Boon W.C., Simpson E.R., Handa R.J., and Rissman E.F. Dietary phytoestrogens dampen female sexual behavior in mice with a disrupted aromatase enzyme gene. Behav. Neurosci. 121 (2007) 356-361
52. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., van der B.B., and Gustafsson J.A. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139 (1998) 4252-4263
53. Lamprecht S.A., Kohen F., Ausher J., Zor U., and Lindner H.R. Hormonal stimulation of oestradiol-17 beta release from the rat ovary during early postnatal development. J. Endocrinol. 68 (1976) 343-344
54. Leighton P.C., Kitau M.J., Chard T., Gordon Y.B., and Leek A.E. Levels of alpha-fetoprotein in maternal blood as a screening test for fetal neural-tube defect. Lancet 2 (1975) 1012-1015
55. Lephart E.D., West T.W., Weber K.S., Rhees R.W., Setchell K.D., Adlercreutz H., and Lund T.D. Neurobehavioral effects of dietary soy phytoestrogens. Neurotoxicol. Teratol. 24 (2002) 5-16
56. Lisk R.D. Progesterone: biphasic effects on the lordosis response in adult or neonatally gonadectomized rats. Neuroendocrinology 5 (1969) 149-160
57. Mackiewicz A., and Breborowicz J. The in vitro production of alpha-fetoprotein variants by human fetal organs. Oncodev. Biol. Med. 1 (1980) 251-261
58. MacLusky N.J., and Naftolin F. Sexual differentiation of the central nervous system. Science 211 (1981) 1294-1302
59. Malsbury C.W., Kow L.M., and Pfaff D.W. Effects of medial hypothalamic lesions on the lordosis response and other behaviors in female golden hamsters. Physiol. Behav. 19 (1977) 223-237
60. Mathews D., and Edwards D.A. The ventromedial nucleus of the hypothalamus and the hormonal arousal of sexual behaviors in the female rat. Horm. Behav. 8 (1977) 40-51
61. Mathews G.A., Brenowitz E.A., and Arnold A.P. Paradoxical hypermasculinization of the zebra finch song system by an antiestrogen. Horm. Behav. 22 (1988) 540-551
62. McCall A.L., Han S.J., Millington W.R., and Baum M.J. Non-saturable transport of [3H]oestradiol across the blood-brain barrier in female rats is reduced by neonatal serum. J. Reprod. Fertil. 61 (1981) 103-108
63. McCarthy M.M., and Konkle A.T. When is a sex difference not a sex difference?. Front. Neuroendocrinol. 26 (2005) 85-102
64. McEwen B.S., Plapinger L., Chaptal C., Gerlach J., and Wallach G. Role of fetoneonatal estrogen binding proteins in the associations of estrogen with neonatal brain cell nuclear receptors. Brain Res. 96 (1975) 400-406
65. Meijs-Roelofs H.M., Uilenbroek J.T., de Jong F.H., and Welschen R. Plasma oestradiol-17beta and its relationship to serum follicle-stimulating hormone in immature female rats. J. Endocrinol. 59 (1973) 295-304
66. Mizejewski G.J., Muehlemann M., and Dauphinee M. Update of alpha fetoprotein growth-inhibitory peptides as biotherapeutic agents for tumor growth and metastasis. Chemotherapy 52 (2006) 83-90
67. Mizejewski G.J., and Vonnegut M. Characteristics of the androgenization produced in mice by neonatal exposure to alpha-fetoprotein antibodies. Teratology 25 (1982) 351-360
68. Naftolin F., Ryan K.J., Davies I.J., Reddy V.V., Flores F., Petro Z., Kuhn M., White R.J., Takaoka Y., and Wolin L. The formation of estrogens by central neuroendocrine tissues. Recent Prog. Horm. Res. 31 (1975) 295-319
69. Nagel S.C., vom Saal F.S., and Welshons W.V. Developmental effects of estrogenic chemicals are predicted by an in vitro assay incorporating modification of cell uptake by serum. J. Steroid Biochem. Mol. Biol. 69 (1999) 343-357
70. Newby D., Dalgliesh G., Lyall F., and Aitken D.A. Alphafetoprotein and alphafetoprotein receptor expression in the normal human placenta at term. Placenta 26 (2005) 190-200
71. Nunez E.A., Benassayag C., Savu L., Vallette G., and Jayle M.F. Serum binding of some steroid hormones during development in different animal species, discussion of the biological significance of this binding. Ann. Biol. Anim. Biochem. Biophys. 16 (1976) 491-501
72. Pfaff D.W., and Sakuma Y. Deficit in the lordosis reflex of female rats caused by lesions in the ventromedial nucleus of the hypothalamus. J. Physiol. 288 (1979) 203-210
73. Pfaff D.W., Schwartz-Giblin S., McCarthy M.M., and Kow L.-M. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E., and Neill J. (Eds). The Physiology of Reproduction vol. 2 (1994), Raven Press, New York 107-220 Ref Type: Serial (Book,Monograph)
74. Pfeiffer C.A. Sexual differences in the hypophyses and their determination by the gonads. Am. J. Anat. 58 (1936) 195-226
75. Phoenix C.H., Goy R.W., Gerall A.A., and Young W.C. Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65 (1959) 369-382
76. Pierman S., Douhard Q., Balthazart J., Baum M.J., and Bakker J. Attraction thresholds and sex discrimination of urinary odorants in male and female aromatase knockout (ArKO) mice. Horm. Behav. 49 (2006) 96-104
77. Pineiro A., Olivito A.M., and Uriel J. Fixation of polyunsaturated fatty acids by alpha fetoprotein and serum albumin in rats. Comparison with the accumulation of these acids in developing rat brain. C. R. Seances Acad. Sci. D 289 (1979) 1053-1056
78. Plapinger L., and McEwen B.S. Ontogeny of estradiol-binding sites in rat brain. I. Appearance of presumptive adult receptors in cytosol and nuclei. Endocrinology 93 (1973) 1119-1128
79. Plumari L., Viglietti-Panzica C., Allieri F., Honda S., Harada N., Absil P., Balthazart J., and Panzica G.C. Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J. Neuroendocrinol. 14 (2002) 971-978
80. Quadros P.S., Goldstein A.Y., De Vries G.J., and Wagner C.K. Regulation of sex differences in progesterone receptor expression in the medial preoptic nucleus of postnatal rats. J. Neuroendocrinol. 14 (2002) 761-767
81. Quadros P.S., Lopez V., De Vries G.J., Chung W.C., and Wagner C.K. Progesterone receptors and the sexual differentiation of the medial preoptic nucleus. J. Neurobiol. 51 (2002) 24-32
82. Quadros P.S., Pfau J.L., Goldstein A.Y., De Vries G.J., and Wagner C.K. Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology 143 (2002) 3727-3739
83. Raynaud J.P. Influence of rat estradiol binding plasma protein (EBP) on uterotrophic activity. Steroids 21 (1973) 249-258
84. Rubin B.S., and Barfield R.J. Priming of estrous responsiveness by implants of 17 beta-estradiol in the ventromedial hypothalamic nucleus of female rats. Endocrinology 106 (1980) 504-509
85. Rubin B.S., Lenkowski J.R., Schaeberle C.M., Vandenberg L.N., Ronsheim P.M., and Soto A.M. Evidence of altered brain sexual differentiation in mice exposed perinatally to low, environmentally relevant levels of bisphenol A. Endocrinology 147 (2006) 3681-3691
86. Sato T., Matsumoto T., Kawano H., Watanabe T., Uematsu Y., Sekine K., Fukuda T., Aihara K., Krust A., Yamada T., Nakamichi Y., Yamamoto Y., Nakamura T., Yoshimura K., Yoshizawa T., Metzger D., Chambon P., and Kato S. Brain masculinization requires androgen receptor function. Proc. Natl. Acad. Sci. USA 101 (2004) 1673-1678
87. Savu L., Benassayag C., Vallette G., Christeff N., and Nunez E. Mouse alpha 1-fetoprotein and albumin. A comparison of their binding properties with estrogen and fatty acid ligands. J. Biol. Chem. 256 (1981) 9414-9418
88. Schachter B.S., and Toran-Allerand C.D. Intraneuronal alpha-fetoprotein and albumin are not synthesized locally in developing brain. Brain Res. 281 (1982) 93-98
89. Schaefer M.L., Young D.A., and Restrepo D. Olfactory fingerprints for major histocompatibility complex-determined body odors. J. Neurosci. 21 (2001) 2481-2487
90. Sell S., and Becker F.F. Alpha-fetoprotein. J. Natl. Cancer Inst. 60 (1978) 19-26
91. Simerly R.B., Swanson L.W., Handa R.J., and Gorski R.A. Influence of perinatal androgen on the sexually dimorphic distribution of tyrosine hydroxylase-immunoreactive cells and fibers in the anteroventral periventricular nucleus of the rat. Neuroendocrinology 40 (1985) 501-510
92. Simerly R.B., Zee M.C., Pendleton J.W., Lubahn D.B., and Korach K.S. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc. Natl. Acad. Sci. USA 94 (1997) 14077-14082
93. Steward J., and Cygan D. Ovarian hormones act early in development to feminize adult open-field behavior in the rat. Horm. Behav. 14 (1980) 20-32
94. Tilghman S.M., and Belayew A. Transcriptional control of the murine albumin/alpha-fetoprotein locus during development. Proc. Natl. Acad. Sci. USA 79 (1982) 5254-5257
95. Tobet S.A., and Baum M.J. Role for prenatal estrogen in the development of masculine sexual behavior in the male ferret. Horm. Behav. 21 (1987) 419-429
96. Tobet S.A., and Hanna I.K. Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell. Mol. Neurobiol. 17 (1997) 565-601
97. Toda K., Takeda K., Okada T., Akira S., Saibara T., Kaname T., Yamamura K., Onishi S., and Shizuta Y. Targeted disruption of the aromatase P450 gene (Cyp19) in mice and their ovarian and uterine responses to 17beta-oestradiol. J. Endocrinol. 170 (2001) 99-111
98. Toran-Allerand C.D. Regional differences in intraneuronal localization of alpha-fetoprotein in developing mouse brain. Brain Res. 281 (1982) 213-217
99. Toran-Allerand C.D. On the genesis of sexual differentiation of the central nervous system: morphogenetic consequences of steroidal exposure and possible role of alpha-fetoprotein. In: De Vries G.J., De Bruin J.P.C., Uylings H.B.M., and Corner M.A. (Eds). Progress in Brain Research. Sex differences in the brain, the relation between structure and function 61 (1984), Elsevier, Amsterdam 63-98 Ref Type: Serial (Book,Monograph)
100. Toran-Allerand C.D. Neuronal uptake of alpha-fetoprotein (AFP) synthesized and secreted by hepatocytes in liver/brain co-cultures. Neurosci. Lett. 83 (1987) 35-40
101. Uriel J., de Nechaud B., and Dupiers M. Estrogen-binding properties of rat, mouse and man fetospecific serum proteins. Demonstration by immuno-autoradiographic methods. Biochem. Biophys. Res. Commun. 46 (1972) 1175-1180
102. Vakharia D., and Mizejewski G.J. Human alpha-fetoprotein peptides bind estrogen receptor and estradiol, and suppress breast cancer. Breast Cancer Res. Treat. 63 (2000) 41-52
103. Vallette G., Benassayag C., Savu L., Delorme J., Nunez E.A., Doumas J., Maume G., and Maume B.F. The serum competitor of oestrogen-rat alpha 1-foetoprotein interactions. Identification as a mixture of non-esterified fatty acids. Biochem. J. 187 (1980) 851-856
104. vom Saal F.S., Grant W.M., McMullen C.W., and Laves K.S. High fetal estrogen concentrations: correlation with increased adult sexual activity and decreased aggression in male mice. Science 220 (1983) 1306-1309
105. Wagner C.K., Pfau J.L., De Vries G.J., and Merchenthaler I.J. Sex differences in progesterone receptor immunoreactivity in neonatal mouse brain depend on estrogen receptor alpha expression. J. Neurobiol. 47 (2001) 176-182
106. Wagner C.K., Xu J., Pfau J.L., Quadros P.S., De Vries G.J., and Arnold A.P. Neonatal mice possessing an Sry transgene show a masculinized pattern of progesterone receptor expression in the brain independent of sex chromosome status. Endocrinology 145 (2004) 1046-1049
107. Wallen K. Hormonal influences on sexually differentiated behavior in nonhuman primates. Front. Neuroendocrinol. 26 (2005) 7-26
108. Weniger J.P. Estrogen production by fetal rat gonads. J. Steroid Biochem. Mol. Biol. 44 (1993) 459-462
109. Weniger J.P., Zeis A., and Chouraqui J. Estrogen production by fetal and infantile rat ovaries. Reprod. Nutr. Dev. 33 (1993) 129-136
110. Wersinger S.R., Haisenleder D.J., Lubahn D.B., and Rissman E.F. Steroid feedback on gonadotropin release and pituitary gonadotropin subunit mRNA in mice lacking a functional estrogen receptor alpha. Endocrine 11 (1999) 137-143
111. Wersinger S.R., Sannen K., Villalba C., Lubahn D.B., Rissman E.F., and De Vries G.J. Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm. Behav. 32 (1997) 176-183
112. Wesson D.W., Keller M., Douhard Q., Baum M.J., and Bakker J. Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm. Behav. 49 (2006) 580-586
113. Whalen R.E., and Edwards D.A. Hormonal determinants of the development of masculine and feminine behavior in male and female rats. Anat. Rec. 157 (1967) 173-180
114. Whitten P.L., Patisaul H.B., and Young L.J. Neurobehavioral actions of coumestrol and related isoflavonoids in rodents. Neurotoxicol. Teratol. 24 (2002) 47-54
115. Wiegand S.J., and Terasawa E. Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology 34 (1982) 395-404
116. Witcher J.A., and Clemens L.G. A prenatal source for defeminization of female rats is the maternal ovary. Horm. Behav. 21 (1987) 36-43